Scientific Papers. Series A. Agronomy, Vol. LXI, No. 1, 2018 ISSN 2285-5785; ISSN CD-ROM 2285-5793; ISSN Online 2285-5807; ISSN-L 2285-5785

FIRST RECORDS OF NATURAL ENEMIES OF HERMONENSIS SPODEK & BEN-DOV (: : ) IN TURKEY

Hasan MARAL1, Halil BOLU2

1Karacadag Development Agency, Urfa Bulvarı No. 19/B, Baglar, Diyarbakir, Turkey 2Dicle University, Faculty of Agriculture, Department of Plant Protection, 21280, Sur, Diyarbakir, Turkey

Corresponding author email: [email protected]

Abstract

This study was carried out on Quercus infectoria Oliv. (Fagaceae) trees infested with the coccid Kermes hermonensis Spodek & Ben-Dov (Hemiptera: Sternorrhyncha: Kermesidae) between 2013 and 2014, in Diyarbakır. As a result of the study, two parasitoids and two predators were obtained. These are: claviger Thomson, 1876; sp. (: : ) and Brumus (Exochomus) quadripustulatus (Linnaeus, 1758), Chilocorus bipustulatus (L.) (Coleoptera: Coccinellidae). B. (Exochomus) quadripustulatus and C. bipustulatus are the first records on K. hermonensis as predators in Turkey. K. hermonensis: Cheiloneurus claviger and Metaphycus sp. are the first records on K. hermonensis as parasitoids in Turkey.

Key words: Kermes hermonensis, Cheiloneurus claviger, Metaphycus sp., Brumus (Exochomus) quadripustulatus, Chilocorus bipustulatus, Turkey.

INTRODUCTION Kermesidae species in Turkey. The other members of the family Nidularia balackhowskii Kermesidae family (Kermesidae: Hemiptera) were found recently on Quercus spp. in many with 91 species in 9 genera (1 fossil species in places. (Ülgentürk et al., 2013). Kermes 1 fossil genus) generally specialized on the hermonensis Spodek & Ben-Dov was described plants belonging to Fagaceae. Family of as a new species in Turkey by Kaydan et al. Kermes Boitard genus is the richest species in (2014). the world as well as in Palaearctic region with Scale family species Kermesidae 33 species (Ben-Dov et al., 2013; Spodek, Ben- (Hemiptera: Coccoidea) are restricted to the Dov, 2014). All species were recorded on northern hemisphere and they are distributed Quercus spp. Although in general for all scale throughout the Nearctic, Oriental and insect, almost all of the description of Kermes Palaearctic regions (Ben-Dov et al., 2015). The species based on adult female stages, first instar family contains about one hundred valid stages were used for the systematic studies as species in ten genera and the majority of well (Bodenheimer, 1953; Balachowsky, 1950, species of the family are known to develop 1953; Borchsenius, 1960; Pellizzari et al., exclusively on Quercus species (Fagaceae) 2012; Spodek, Ben-Dov, 2014). (Ben-Dov et al., 2015). Females and males Ten species have been recorded up to now develop mainly on twigs, branches and in bark belonging to genus Kermes and Nidularia crevices, while some species develop on leaves Targioni-Tozzetti in Turkey (Ülgenturk et al. (Sternlicht, 1969; Bullington, Kosztarab, 1985; 2013). Bodenheimer himself described three Hu, 1986; Podsiadlo, 2005). Kermes species in Turkey between 1951 and Most Kermesidae species are not known that 1953, but unfortunately either the type material they cause any visible damage to their host and dry materials are not in good conditions trees. However there are reports of infestations and they need more attention indeed. Although of some species that have led to branch K. bekirii Bodenheimer, K. muhlisi dieback, flagging, reduced growth rates and Bodenheimer, K. sadrii Bodenheimer and K. occasionally tree death. These occurrences are safinazae Özkök were described from Turkey, mainly in urban areas (Kozár, 1974; Hamon, there are not complementary studies on the 1977; Solomon et al., 1980; Viggiani, 1991; 334

Pellizzari et al., 2012; Podsiadlo, 2012). Asterolecaniidae (pit scales) (Anonymous Kermesidae species belong to two genera 2016a). named Nidularia Targioni-Tozzetti and Kermes The aim of this study was to determine the Boitard in the Mediterranean and European natural enemies of the harmful Kermes regions. Species of Kermes (Hemiptera: hermonensis on Quercus infectoria trees in Kermesidae) are specialist sap-feeders on Diyarbakır. species of Quercus and they can be economically important at high population MATERIALS AND METHODS densities. On the other hand, these can be Soft samples were collected from important for honey bees in honey production. the province of Diyarbakır in the Southeastern Among the most important natural enemies of Part of Turkey in 2013. Specimens were taken Kermes species are encyrtids within the genus from both wild and cultivated plants during Psilophrys (Japoshvili, 2005; Japoshvili, irregular surveys carried out in the spring and Noyes, 2006a). However, there are some summer seasons of the one-year study. Each Blastothrix species that also parasitize Kermes sample was put into a plastic bag and taken to spp. (Trjapitzin, 1989; Japoshvili, Karaca, the laboratory for examination. 2003). Undoubtedly, these parasitoids have an Representative specimens were sent to various important effect on scale about the population taxonomic specialists for confirmation of of the species. identification. Host identification (Kermes The Encyrtidae constitute the majority of hermonensis) was made by Dr. Malkie Spodek parasitoids attacking to the psyllid insects. (Department of Entomology, Agricultural Members of the family are important in Research Organization The Volcani Center, biological control. More than 400 encyrtid P.O. Box 6, Bet Dagan, 50250 ISRAEL), the species have been used or are used today for coccinellids identification was made by Prof. suppression of various crop pests (Japoshvili, Dr. Nedim Uygun (Çukurova University, Noyes, 2006b). There are more than 1270 Faculty of Agriculture, Department of Plant described species of encyrtids in the Palaearctic Protection, 01330 Adana, Turkey) and the Region (Yasnosh, Japoshvili, 1999; Japoshvili, parasitoids identification was made by Prof. Dr. 2005-2007a, b; Japoshvili, Karaca, 2003; George Joposhvili (Institute of Entomology Japoshvili, Noyes 2005-2006b). agricultural University of Georgia-Georgia). The Coccinellidae are generally considered as Samples were collected from ornamental plants an useful insects, because many species of it from Diyarbakır in Turkey. Each sample was feed on aphids which are pests in gardens, placed into a plastic bag and taken to the agricultural fields, orchards, and similar places. laboratory for examination. Colonies of such plant-eating pests lay hundreds of eggs and then the larvae RESULTS AND DISCUSSIONS commences feeding immediately. However, some species do have unwelcome effects; As a result of this study, two parasitoids among these, the most prominent are the species Cheiloneurus claviger Thomson, 1876, subfamily Epilachninae, which are plant eaters. Metaphycus sp. (Hymenoptera: Encyrtidae: Thirteen genera contain 66 species that are Encyrtinae) and two predators species Brumus placed here into this large trophic group that (Exochomus) quadripustulatus (Linnaeus, has scale insects as its prey. Members of the 1758), Chilocorus bipustulatus (Linnaeus, superfamily Coccoidea (the scale insects); this 1758). (Coleoptera: Coccinellidae) were superfamily includes various related families, obtained. notably Coccidae (soft scales), Diaspididae Kermes hermonensis Spodek, Ben-Dov (armored scales), Pseudococcidae (mealybugs), (Hemiptera: Sternorrhyncha: Kermesidae) Dactylopiidae ( scales), Kermesidae Distribution in World: Israel (Spodek, Ben- (gall-like scales), Eriococcidae (felt scales), Dov, 2014), Cerococcidae (ornate pit scales), and Distribution in Turkey: Diyarbakır (Kaydan et al., 2014).

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Host plant: Quercus species (Fagaceae) (Ben- New record host in Turkey. In the present Dov et al. 2015), Quercus infectoria Oliv. study Kermes hermonensis was recorded as a (Fagaceae) (Kaydan et al., 2014). new host of Metaphycus sp. for Turkey. Material examined: Diyarbakır (38o 09’ 41o Material examined: 2♀♀ Locality: Diyarbakır 12’ 54’E at altitude of about 663 m.). (Diyarbakır 38o 09’41o 12’ 54’E at altitude of Cheiloneurus claviger Thomson, 1876 about 663 m.). (Hymenoptera: Encyrtidae: Encyrtinae) Brumus (Exochomus) quadripustulatus Recorded hosts: Acanthopulvinaria orientalis (Linnaeus, 1758) (Coleoptera: Coccinellidae) (Nasonov) (Coccidae: Acanthopulvinaria) Recorded hosts. The pine ladybird a (Japoshvili, Çelik, 2010; Myartseva, 1984); polyphagous predatory in both adult and larval Ceroplastes ceriferus (Fabricius) (Hemiptera, stages preys aphids and scale insects (Uygun, Coccidae) (Japoshvili, Çelik, 2010; Xu, Huang, 1981; Çelik, 1983; Bolu, 2002; Bolu, 2004; 2004); Ceroplastes japonicus Green Bolu et al., 2007). (Hemiptera: Coccoidea: Coccidae) (Japoshvili, New record host in World. In the present Çelik, 2010; Japoshvili, Noyes, 2005; study Kermes hermonensis was recorded as a Japoshvili, 2000); Chloropulvinaria aurantii new host of Brumus (Exochomus) (Cockerell) (Hemiptera: Coccidae) (Xu, quadripustulatus from Turkey for world. Huang, 2004); Coccus hesperidum L. Distribution in World: Albania, Austria, (Hemiptera: Coccoidea: Coccidae) (Japoshvili, Balearic Is., Belarus, Belgium, Bosnia and Çelik, 2010); Kermes hermonensis Spodek, Herzegovina, Britain I., Bulgaria, Corsica, Ben-Dov (Hemiptera: Sternorrhyncha: Crete, Croatia, Cyprus, Czech Republic, Danish Kermesidae) (Japoshvili et al., 2015); Kermes mainland, Estonia, European Turkey, Finland, vermilio Planchon (Hemiptera: French mainland, Germany, Greek mainland, Sternorrhyncha: Kermesidae) (Japoshvili, Hungary, Italian mainland, Latvia, Lithuania, Çelik, 2010; Marotta et al., 1999) Luxembourg, Macedonia, Moldova, Norwegian New record host in Turkey: In the present mainland, Poland, Portuguese mainland, study Kermes hermonensis was recorded as a Romania, Russia Central, Russia North, Russia new host of Cheiloneurus claviger in Turkey. South, San Marino, Sardinia, Sicily, Slovakia, Distribution: Armenia, Austria, Azerbaijan, Slovenia, Spanish mainland, Sweden, Bulgaria, Croatia, Czech Republic, Switzerland, Netherlands, Ukraine, Yugoslavia Czechoslovakia, Egypt, Europe, France, (Anonymous, 2016b). Georgia, Germany, Greece, Hungary, Iran, Distribution in Turkey: Balıkesir, Denizli, Israel, Italy, Japan, Kazakhstan, Moldova, İzmir (Giray, 1970); Aegean Region Montenegro, Netherlands, Palaearctic, (Soydanbay-Tunçyürek, 1976); Artvin, Rize Romania, Russia, Serbia, Slovakia, Spain, (Bozan, Aslıtürk, 1975); İzmir (Öncüer, 1977); Sweden, Tadzhikistan, Transcaucasus, Turkey, Eastern Mediterranean Region (Uygun, 1981); Turkmenistan, Ukraine, United Kingdom, Ankara (Düzgüneş et al., 1982); Gaziantep USSR, Uzbekistan, Yugoslavia (Federal (Çelik, 1983); Erzurum (Özbek, Çetin, 1991); Republic) (Anonymous, 2016b). Southeastern Anatolia Region (Bolu, Uygun, Material examined: 2♀♀ Locality: Diyarbakır 2003; Bolu, 2002-2004; Bolu et al., 2007); (Diyarbakır 38o 09’ 41o 12’ 54’E at altitude of Adana, Niğde (Ulusoy et al., 1999); Diyarbakır, about 663 m.). Elazığ, Mardin (Bolu, 2005). Metaphycus sp. (Hymenoptera: Encyrtidae: Material examined: 10 adult ladybirds was Encyrtinae) obtained in total. Target Pests: Soft brown scale, black scale and Locality: Diyarbakır (Diyarbakır 38o 09’ 41o citricola scale. 12’ 54’ E at altitude of about 663 m.). Crops suitable: Citrus, olives, passion fruit, Chilocorus bipustulatus (L.) (Coleoptera: figs, custard apples and a wide range of Coccinellidae) ornamentals including gardenia, oleander, ferns Recorded hosts: Heather ladybirds feed on and palms. aphids and scale insects, small insects mainly belonging to the family of Coccidae and

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